Anti-rotavirus Properties and Mechanisms of Selected Gram-Positive and Gram-Negative Probiotics on Polarized Human Colonic (HT-29) Cells

Anand Kumar, Yosra A. Helmy, Zachary Fritts, Anastasia Vlasova, Linda J. Saif, Gireesh Rajashekara

Research output: Contribution to journalArticlepeer-review

6 Scopus citations

Abstract

Probiotics have been investigated to improve the universal rotavirus (RV) vaccination as well as to ameliorate the RV infection. However, underlying mechanisms how probiotics mediate beneficial effects needs more investigation. Thus, in the present study, we used polarized HT-29 cells to assess the anti-RV properties of Gram-positive, (Lactobacillus acidophilus, Lacticaseibacillus rhamnosus GG, and Bifidobacterium subsp. Lactis Bb12) and Gram negative, (Escherichia coli Nissle 1917) probiotics and study their underlying mechanisms. Our results showed that pre-treatment of HT-29 cells for 4 h with probiotics, significantly reduced (p < 0.05) human RV replication and this effect was most pronounced for E. coli Nissle followed by L. acidophilus and L. rhamnosus GG. Strikingly, only pre-treatment with live bacteria or their supernatants demonstrated anti-RV properties. Except Gram negative E. coli Nissle, the Gram-positive probiotics tested did not bind to RV. Ingenuity pathway analysis of tight junction (TJ)- and innate immune-associated genes indicated that E. coli Nissle or E. coli Nissle + RV treatments improved cell–cell adhesion and cell contact, while L. acidophilus or L. acidophilus + RV treatments also activated cell–cell contact but inhibited cell movement functions. RV alone inhibited migration of cells event. Additionally, E. coli Nissle activated pathways such as the innate immune and inflammatory responses via production of TNF, while RV infection activated NK cells and inflammatory responses. In conclusion, E. coli Nissle’s ability to bind RV, modulate expression of TJ events, innate immune and inflammatory responses, via specific upstream regulators may explain superior anti-RV properties of E. coli Nissle. Therefore, prophylactic use of E. coli Nissle might help to reduce the RV disease burden in infants in endemic areas.

Original languageEnglish
Pages (from-to)107-128
Number of pages22
JournalProbiotics and Antimicrobial Proteins
Volume15
Issue number1
DOIs
StateAccepted/In press - 2022

Bibliographical note

Funding Information:
This work was supported by the Bill and Melinda Gates Foundation (OPP 1117467), the NIAID, NIH (R01 A1099451), federal and state funds appropriated to the Ohio Agricultural Research and Development Center, The Ohio State University and from the NIH Office of Dietary Supplements (ODS) supplemental grant funds.

Publisher Copyright:
© 2021, The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.

Funding

This work was supported by the Bill and Melinda Gates Foundation (OPP 1117467), the NIAID, NIH (R01 A1099451), federal and state funds appropriated to the Ohio Agricultural Research and Development Center, The Ohio State University and from the NIH Office of Dietary Supplements (ODS) supplemental grant funds. Authors thank Dr. Sukumar Kandasamy and Tea Meulia for their technical assistance in performing rotavirus binding assay and electron microscopy imaging, respectively.

FundersFunder number
Tea Meulia, Molecular and Cellular Imaging Center
National Institutes of Health (NIH)R01 A1099451
National Institute of Allergy and Infectious Diseases
Office of Dietary Supplements
Bill and Melinda Gates FoundationOPP 1117467
Ohio Water Resources Center, Ohio State University
Ohio Agricultural Research and Development Center, Ohio State University

    Keywords

    • E. coli Nissle
    • HT-29 cells
    • Innate immune response
    • Probiotics
    • Rotavirus
    • Tight junction

    ASJC Scopus subject areas

    • Microbiology
    • Molecular Medicine
    • Molecular Biology

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